Porphyromonas gingivalis and Treponema denticola synergistic polymicrobial biofilm development
Chronic periodontitis has a polymicrobial biofilm aetiology and interactions between key bacterial species are strongly implicated as contributing to disease progression. Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia have all been implicated as playing roles in disease progr...
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| description | Chronic periodontitis has a polymicrobial biofilm aetiology and interactions between key bacterial species are strongly implicated as contributing to disease progression. Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia have all been implicated as playing roles in disease progression. P. gingivalis cell-surface-located protease/adhesins, the gingipains, have been suggested to be involved in its interactions with several other bacterial species. The aims of this study were to determine polymicrobial biofilm formation by P. gingivalis, T. denticola and T. forsythia, as well as the role of P. gingivalis gingipains in biofilm formation by using a gingipain null triple mutant. To determine homotypic and polymicrobial biofilm formation a flow cell system was employed and the biofilms imaged and quantified by fluorescent in situ hybridization using DNA species-specific probes and confocal scanning laser microscopy imaging. Of the three species, only P. gingivalis and T. denticola formed mature, homotypic biofilms, and a strong synergy was observed between P. gingivalis and T. denticola in polymicrobial biofilm formation. This synergy was demonstrated by significant increases in biovolume, average biofilm thickness and maximum biofilm thickness of both species. In addition there was a morphological change of T. denticola in polymicrobial biofilms when compared with homotypic biofilms, suggesting reduced motility in homotypic biofilms. P. gingivalis gingipains were shown to play an essential role in synergistic polymicrobial biofilm formation with T. denticola. |
| doi_str_mv | 10.1371/journal.pone.0071727 |
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Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia have all been implicated as playing roles in disease progression. P. gingivalis cell-surface-located protease/adhesins, the gingipains, have been suggested to be involved in its interactions with several other bacterial species. The aims of this study were to determine polymicrobial biofilm formation by P. gingivalis, T. denticola and T. forsythia, as well as the role of P. gingivalis gingipains in biofilm formation by using a gingipain null triple mutant. To determine homotypic and polymicrobial biofilm formation a flow cell system was employed and the biofilms imaged and quantified by fluorescent in situ hybridization using DNA species-specific probes and confocal scanning laser microscopy imaging. Of the three species, only P. gingivalis and T. denticola formed mature, homotypic biofilms, and a strong synergy was observed between P. gingivalis and T. denticola in polymicrobial biofilm formation. This synergy was demonstrated by significant increases in biovolume, average biofilm thickness and maximum biofilm thickness of both species. In addition there was a morphological change of T. denticola in polymicrobial biofilms when compared with homotypic biofilms, suggesting reduced motility in homotypic biofilms. P. gingivalis gingipains were shown to play an essential role in synergistic polymicrobial biofilm formation with T. denticola.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0071727</identifier><identifier>PMID: 23990979</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adhesins ; Adhesins, Bacterial - genetics ; Adhesins, Bacterial - metabolism ; Bacteria ; Biofilms ; Biofilms - growth & development ; Biology ; Borrelia burgdorferi ; Cell surface ; Chronic Periodontitis - microbiology ; Cysteine Endopeptidases - genetics ; Cysteine Endopeptidases - metabolism ; Dental schools ; Deoxyribonucleic acid ; Disease ; DNA ; DNA probes ; Fluorescence ; Fluorescence in situ hybridization ; Fluorescent indicators ; Gingipain ; Hemoglobin ; In Situ Hybridization, Fluorescence ; Laser microscopy ; Medicine ; Microscopy ; Microscopy, Confocal ; Microscopy, Electron, Scanning ; Morphology ; Motility ; Mutation ; Oral hygiene ; Periodontitis ; Porphyromonas gingivalis ; Porphyromonas gingivalis - genetics ; Porphyromonas gingivalis - physiology ; Porphyromonas gingivalis - ultrastructure ; Species ; Species Specificity ; Treponema - genetics ; Treponema - physiology ; Treponema - ultrastructure ; Treponema denticola ; Treponema denticola - genetics ; Treponema denticola - physiology ; Treponema denticola - ultrastructure</subject><ispartof>PloS one, 2013-08, Vol.8 (8), p.e71727-e71727</ispartof><rights>2013 Zhu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Zhu et al 2013 Zhu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-c06580dffbc483160c3d58c89bcfc57f93089802d8e0bb91254c6d44a3133d383</citedby><cites>FETCH-LOGICAL-c526t-c06580dffbc483160c3d58c89bcfc57f93089802d8e0bb91254c6d44a3133d383</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3753311/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3753311/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23990979$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Brissette, Catherine A.</contributor><creatorcontrib>Zhu, Ying</creatorcontrib><creatorcontrib>Dashper, Stuart G</creatorcontrib><creatorcontrib>Chen, Yu-Yen</creatorcontrib><creatorcontrib>Crawford, Simon</creatorcontrib><creatorcontrib>Slakeski, Nada</creatorcontrib><creatorcontrib>Reynolds, Eric C</creatorcontrib><title>Porphyromonas gingivalis and Treponema denticola synergistic polymicrobial biofilm development</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Chronic periodontitis has a polymicrobial biofilm aetiology and interactions between key bacterial species are strongly implicated as contributing to disease progression. Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia have all been implicated as playing roles in disease progression. P. gingivalis cell-surface-located protease/adhesins, the gingipains, have been suggested to be involved in its interactions with several other bacterial species. The aims of this study were to determine polymicrobial biofilm formation by P. gingivalis, T. denticola and T. forsythia, as well as the role of P. gingivalis gingipains in biofilm formation by using a gingipain null triple mutant. To determine homotypic and polymicrobial biofilm formation a flow cell system was employed and the biofilms imaged and quantified by fluorescent in situ hybridization using DNA species-specific probes and confocal scanning laser microscopy imaging. Of the three species, only P. gingivalis and T. denticola formed mature, homotypic biofilms, and a strong synergy was observed between P. gingivalis and T. denticola in polymicrobial biofilm formation. This synergy was demonstrated by significant increases in biovolume, average biofilm thickness and maximum biofilm thickness of both species. In addition there was a morphological change of T. denticola in polymicrobial biofilms when compared with homotypic biofilms, suggesting reduced motility in homotypic biofilms. P. gingivalis gingipains were shown to play an essential role in synergistic polymicrobial biofilm formation with T. denticola.</description><subject>Adhesins</subject><subject>Adhesins, Bacterial - genetics</subject><subject>Adhesins, Bacterial - metabolism</subject><subject>Bacteria</subject><subject>Biofilms</subject><subject>Biofilms - growth & development</subject><subject>Biology</subject><subject>Borrelia burgdorferi</subject><subject>Cell surface</subject><subject>Chronic Periodontitis - microbiology</subject><subject>Cysteine Endopeptidases - genetics</subject><subject>Cysteine Endopeptidases - metabolism</subject><subject>Dental schools</subject><subject>Deoxyribonucleic acid</subject><subject>Disease</subject><subject>DNA</subject><subject>DNA probes</subject><subject>Fluorescence</subject><subject>Fluorescence in situ hybridization</subject><subject>Fluorescent indicators</subject><subject>Gingipain</subject><subject>Hemoglobin</subject><subject>In Situ Hybridization, Fluorescence</subject><subject>Laser microscopy</subject><subject>Medicine</subject><subject>Microscopy</subject><subject>Microscopy, Confocal</subject><subject>Microscopy, Electron, Scanning</subject><subject>Morphology</subject><subject>Motility</subject><subject>Mutation</subject><subject>Oral hygiene</subject><subject>Periodontitis</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - genetics</subject><subject>Porphyromonas gingivalis - physiology</subject><subject>Porphyromonas gingivalis - ultrastructure</subject><subject>Species</subject><subject>Species Specificity</subject><subject>Treponema - genetics</subject><subject>Treponema - physiology</subject><subject>Treponema - ultrastructure</subject><subject>Treponema denticola</subject><subject>Treponema denticola - genetics</subject><subject>Treponema denticola - physiology</subject><subject>Treponema denticola - ultrastructure</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUk1v3CAQRVWjJt32H1StpV562Q0wNoZLpSjqR6RIySG9FmHADisMLuyutP--bNaJkqpcYOC9x7yZQegDwSsCLTlfx20Kyq-mGOwK45a0tH2FzogAumQUw-tn51P0Nuc1xg1wxt6gUwpCYNGKM_T7Nqbpfp_iGIPK1eDC4HbKu1ypYKq7ZA_yo6qMDRuno1dV3gebBpdLWE3R70enU-yc8lXnYu_8WLA76-M0Fso7dNIrn-37eV-gX9-_3V3-XF7f_Li6vLhe6oayzVJj1nBs-r7TNQfCsAbTcM1Fp3vdtL0AzAXH1HCLu04Q2tSambpWQAAMcFigT0fdyccs59JkSWrKMcMgaEFcHREmqrWckhtV2suonHy4iGmQKhVP3kpKCSOlPpQpXuNWc2t4zzkojUFZ0xWtr_Nv2260RhejSfkXoi9fgruXQ9xJaBsAQorAl1kgxT9bmzdydFlb71WwcfuQt6CkhrIW6PM_0P-7q4-o0ouck-2fkiFYHsblkSUP_ZTzuBTax-dGnkiP8wF_ARqbv94</recordid><startdate>20130826</startdate><enddate>20130826</enddate><creator>Zhu, Ying</creator><creator>Dashper, Stuart G</creator><creator>Chen, Yu-Yen</creator><creator>Crawford, Simon</creator><creator>Slakeski, Nada</creator><creator>Reynolds, Eric C</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130826</creationdate><title>Porphyromonas gingivalis and Treponema denticola synergistic polymicrobial biofilm development</title><author>Zhu, Ying ; Dashper, Stuart G ; Chen, Yu-Yen ; Crawford, Simon ; Slakeski, Nada ; Reynolds, Eric C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-c06580dffbc483160c3d58c89bcfc57f93089802d8e0bb91254c6d44a3133d383</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adhesins</topic><topic>Adhesins, Bacterial - genetics</topic><topic>Adhesins, Bacterial - metabolism</topic><topic>Bacteria</topic><topic>Biofilms</topic><topic>Biofilms - growth & development</topic><topic>Biology</topic><topic>Borrelia burgdorferi</topic><topic>Cell surface</topic><topic>Chronic Periodontitis - microbiology</topic><topic>Cysteine Endopeptidases - genetics</topic><topic>Cysteine Endopeptidases - metabolism</topic><topic>Dental schools</topic><topic>Deoxyribonucleic acid</topic><topic>Disease</topic><topic>DNA</topic><topic>DNA probes</topic><topic>Fluorescence</topic><topic>Fluorescence in situ hybridization</topic><topic>Fluorescent indicators</topic><topic>Gingipain</topic><topic>Hemoglobin</topic><topic>In Situ Hybridization, Fluorescence</topic><topic>Laser microscopy</topic><topic>Medicine</topic><topic>Microscopy</topic><topic>Microscopy, Confocal</topic><topic>Microscopy, Electron, Scanning</topic><topic>Morphology</topic><topic>Motility</topic><topic>Mutation</topic><topic>Oral hygiene</topic><topic>Periodontitis</topic><topic>Porphyromonas gingivalis</topic><topic>Porphyromonas gingivalis - genetics</topic><topic>Porphyromonas gingivalis - physiology</topic><topic>Porphyromonas gingivalis - ultrastructure</topic><topic>Species</topic><topic>Species Specificity</topic><topic>Treponema - genetics</topic><topic>Treponema - physiology</topic><topic>Treponema - ultrastructure</topic><topic>Treponema denticola</topic><topic>Treponema denticola - genetics</topic><topic>Treponema denticola - physiology</topic><topic>Treponema denticola - ultrastructure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhu, Ying</creatorcontrib><creatorcontrib>Dashper, Stuart G</creatorcontrib><creatorcontrib>Chen, Yu-Yen</creatorcontrib><creatorcontrib>Crawford, Simon</creatorcontrib><creatorcontrib>Slakeski, Nada</creatorcontrib><creatorcontrib>Reynolds, Eric C</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhu, Ying</au><au>Dashper, Stuart G</au><au>Chen, Yu-Yen</au><au>Crawford, Simon</au><au>Slakeski, Nada</au><au>Reynolds, Eric C</au><au>Brissette, Catherine A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Porphyromonas gingivalis and Treponema denticola synergistic polymicrobial biofilm development</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-08-26</date><risdate>2013</risdate><volume>8</volume><issue>8</issue><spage>e71727</spage><epage>e71727</epage><pages>e71727-e71727</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Chronic periodontitis has a polymicrobial biofilm aetiology and interactions between key bacterial species are strongly implicated as contributing to disease progression. Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia have all been implicated as playing roles in disease progression. P. gingivalis cell-surface-located protease/adhesins, the gingipains, have been suggested to be involved in its interactions with several other bacterial species. The aims of this study were to determine polymicrobial biofilm formation by P. gingivalis, T. denticola and T. forsythia, as well as the role of P. gingivalis gingipains in biofilm formation by using a gingipain null triple mutant. To determine homotypic and polymicrobial biofilm formation a flow cell system was employed and the biofilms imaged and quantified by fluorescent in situ hybridization using DNA species-specific probes and confocal scanning laser microscopy imaging. Of the three species, only P. gingivalis and T. denticola formed mature, homotypic biofilms, and a strong synergy was observed between P. gingivalis and T. denticola in polymicrobial biofilm formation. This synergy was demonstrated by significant increases in biovolume, average biofilm thickness and maximum biofilm thickness of both species. In addition there was a morphological change of T. denticola in polymicrobial biofilms when compared with homotypic biofilms, suggesting reduced motility in homotypic biofilms. P. gingivalis gingipains were shown to play an essential role in synergistic polymicrobial biofilm formation with T. denticola.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23990979</pmid><doi>10.1371/journal.pone.0071727</doi><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-08, Vol.8 (8), p.e71727-e71727 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1428060392 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adhesins Adhesins, Bacterial - genetics Adhesins, Bacterial - metabolism Bacteria Biofilms Biofilms - growth & development Biology Borrelia burgdorferi Cell surface Chronic Periodontitis - microbiology Cysteine Endopeptidases - genetics Cysteine Endopeptidases - metabolism Dental schools Deoxyribonucleic acid Disease DNA DNA probes Fluorescence Fluorescence in situ hybridization Fluorescent indicators Gingipain Hemoglobin In Situ Hybridization, Fluorescence Laser microscopy Medicine Microscopy Microscopy, Confocal Microscopy, Electron, Scanning Morphology Motility Mutation Oral hygiene Periodontitis Porphyromonas gingivalis Porphyromonas gingivalis - genetics Porphyromonas gingivalis - physiology Porphyromonas gingivalis - ultrastructure Species Species Specificity Treponema - genetics Treponema - physiology Treponema - ultrastructure Treponema denticola Treponema denticola - genetics Treponema denticola - physiology Treponema denticola - ultrastructure |
| title | Porphyromonas gingivalis and Treponema denticola synergistic polymicrobial biofilm development |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-31T10%3A41%3A03IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Porphyromonas%20gingivalis%20and%20Treponema%20denticola%20synergistic%20polymicrobial%20biofilm%20development&rft.jtitle=PloS%20one&rft.au=Zhu,%20Ying&rft.date=2013-08-26&rft.volume=8&rft.issue=8&rft.spage=e71727&rft.epage=e71727&rft.pages=e71727-e71727&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0071727&rft_dat=%3Cproquest_plos_%3E1429214333%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1428060392&rft_id=info:pmid/23990979&rft_doaj_id=oai_doaj_org_article_2216190926a8407c8ed8f883ac03aedb&rfr_iscdi=true |